Biotic interaction between spionid polychaetes and bouchardiid brachiopods: Paleoecological, taphonomic and evolutionary implications

SABRINA C. RODRIGUES, MARCELLO G. SIMÕES, MICHAŁ KOWALEWSKI, MÔNICA A.V. PETTI, EDMUNDO F. NONATO, SERGIO MARTINEZ, and CLAUDIA JULIA DEL RIO

Rodrigues, S.C., Simões, M.G., Kowalewski, M., Petti, M.A.V., Nonato, E.F., Martinez, S., and del Rio, C.J. 2008. Biotic interaction between spionid polychaetes and bouchardiid brachiopods: Paleoecological, taphonomic and evolutionary implications. Acta Palaeontologica Polonica 53 (4): 657–668.

Shells of Bouchardia rosea (Brachiopoda, Rhynchonelliformea) are abundant in Late Holocene death assemblages of the Ubatuba Bight, Brazil, SW Atlantic. This genus is also known from multiple localities in the Cenozoic fossil record of South America. A total of 1211 valves of B. rosea, 2086 shells of sympatric bivalve mollusks (14 nearshore localities ranging in depth from 0 to 30 m), 80 shells of Bouchardia zitteli, San Julián Formation, Paleogene, Argentina, and 135 shells of Bouchardia transplatina, Camacho Formation, Neogene, Uruguay were examined for bioerosion traces. All examined bouchardiid shells represent shallow−water, subtropical marine settings. Out of 1211 brachiopod shells of B. rosea, 1201 represent dead individuals. A total of 149 dead specimens displayed polychaete traces (Caulostrepsis). Live polychaetes were found inside Caulostrepsis borings in 10 life−collected brachiopods, indicating a syn−vivo interaction (Caulostrepsis traces in dead shells of B. rosea were always empty). The long and coiled peristomial palps, large chaetae on both sides of the 5th segment, and flanged pygidium found in the polychaetes are characteristic of the polychaete genus Polydora (Spionidae). The fact that 100% of the Caulostrepsis found in living brachiopods were still inhabited by the trace−making spionids, whereas none was found in dead hosts, implies active biotic interaction between the two living organisms rather than coloni− zation of dead brachiopod shells. The absence of blisters, the lack of valve/site stereotypy, and the fact that tubes open only externally are all suggestive of a commensal relationship. These data document a new host group (bouchardiid rhyncho− nelliform brachiopods) with which spionids can interact (interestingly, spionid−infested sympatric bivalves have not been found in the study area despite extensive sampling). The syn−vivo interaction indicates that substantial bioerosion may occur when the host is alive. Thus, the presence of such bioerosion traces on fossil shells need not imply a prolonged post−mortem exposure of shells on the sea floor. Also, none of the Paleogene and Neogene Bouchardia species included any ichnological evidence for spionid infestation. This indicates that the Spionidae/ Bouchardia association may be geologically young, al− though the lack of older records may also reflect limited sampling and/or taphonomic biases.

Key words: Brachiopoda, Spionidae, Caulostrepsis, Bouchardia, biotic interaction, bioerosion, Cenozoic, Brazil.

Sabrina Rodrigues [[email protected]], Marcello Simões [[email protected]], Departamento de Zoologia, Instituto de Biociências Distrito de Rubião Júnior s/n CxP 510 18618−000 Botucatu, SP Brazil; Michal Kowalewski [[email protected]], Department of Geosciences, Virginia Polytechnic Institute and State University Blacksburg, USA; Mônica Petti [[email protected]], Edmundo Nonato [[email protected]], Departamento de Oceanografia Biologica, Instituto Oceanografico, Praça do Oceanográfico, 191 05508−120 São Paulo, SP Brazil; Sergio Martinez [[email protected]], Facultad de Ciencias, Inguá 4225, 11400 Montevideo, Uruguay; Claudia del Rio [[email protected]], Museo Argentino de Ciencias Naturales Bernardino Rivadavia, División Paleoinvertebrados, Angel Gallardo 470, Buenos Aires, Argentina.

Introduction gues et al. 2002), B. rosea shells represent an important sub− strate for boring and encrusting organisms through the Holo− Bouchardia rosea (Mawe, 1823), an endemic, free−living cene (Rodland et al. 2004, 2006; Simões et al. 2007a). brachiopod, epifaunal or quase−infaunal is patchily distrib− Although Bouchardia rosea is the only extant member of uted, but often abundant in the death assemblages of the the Bouchardioidea (MacKinnon and Lee 2006), the fossil southern Brazilian shelf (Tommasi 1970; Kowalewski et al. record of the genus can be traced back all the way to the 2002; Simões et al. 2004a). On the Brazilian inner shelf, a re− Cretaceous/Paleocene boundary in the southern hemisphere gion mainly dominated by siliciclastic bottoms, largely de− (Manceñido and Griffin 1988). In fact, Bouchardia shells void of hard substrates (Mahiques et al. 1998, 2004; Rodri− have been documented in multiple fossil benthic associations

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45o W A 23o 20’S B 20o S Brazil

Uruguay UBA 14

o 40 S Argentina Ubatuba UBA 10 Bay UBA 11 UBA 9 UBA 7 N UBA 12 ATLANTIC OCEAN UBA 8

UBA 5 O O 0 500 km UBA 1 80 W 60 W UBA 6 UBA 3 UBA 2 UBA 4 C

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Palmas Island Anchieta 04km Island

48o S Santa Cruz Province

o 34 30’S La Plata River ATLANTIC OCEAN N

050km N O O 020km 60 W 58 W Montevideo

Fig. 1. A schematic map of the study area (A), including present−day sites along the northern coast of São Paulo State (Brazil) (B) as well as the sampled fos− sil localities in Argentina (C) and Uruguay (D). of South America, including Paleogene (San Julián Forma− fossil B. zitteli and B. transplatina species; (iv) compare trace tion, Patagonia, Argentina) and Neogene (Camacho Forma− frequencies on Holocene brachiopod shells with sympatric bi− tion, Uruguay) localities. In these geological units, Bou− valve mollusks; and (v) assess the effect of the bioerosion on chardia−rich accumulations are found in subtropical marine the taphonomic behavior of shells of B. rosea. provinces ranging from intertidal to mid−shelf depositional Institutional abbreviations.—DZP, Departamento de Zoolo− settings. Consequently, Bouchardia shells represent a suit− gia, Instituto de Biociências, Universidade Estadual Paulista, able target for studying long−term patterns in biotic interac− Brazil; FCDP, Departamento de Paleontología, Facultad de tions between brachiopods and boring organisms across sim− Ciencias, Uruguay; IGC−DPE, Departamento de Geologia ilar—subtropical and predominately shallow−water—marine Sedimentar e Ambiental, Instituto de Geociências, Universi− ecosystems of the Cenozoic South America. dade de São Paulo, Brazil. This study aims to: (i) evaluate the identity of the primary bioeroder in living brachiopod shells and discuss possible eco− logical interpretations of this interaction; (ii) describe the traces left by the bioeroders in brachiopod shells to enhance Historical background our ability to recognize such traces in the fossil record and/or in shells found in Holocene death assemblages; (iii) estimate As will be discussed in detail below, all borings found in the trace frequencies for the extant (Bouchardia rosea)and Bouchardia shells are referable to Caulostrepsis. This trace RODRIGUES ET AL.—SPIONID—BRACHIOPODS INTERACTION 659 is known from numerous rockgrounds and shells from the horizons”, named at the beginning of the 20th century. These Devonian to Holocene (see Taylor and Wilson 2003 for a re− horizons were subsequently placed in the San Julián Forma− view). As commented by Bromley (1978, 1994), Caulo− tion and Monte León Formation (Bertels 1970). Ihering (1907) strepsis and its various ichnospecies (e.g., C. taeniola, C. placed the fossiliferous horizons exposed in Manantial Salado cretacea) are most likely to record euendolithic or para− locality in the basal section of the “Patagonian beds” (Fig. 2), endolithic activities of polychaete annelids of various fami− but it is not clear from his paper (Ihering 1907), or from indica− lies, in particular spionid polychaetes (Barrier and D’Ales− tions of labels of his collection, if that locality is situated in the sandro 1985). Although Caulostrepsis is known from shells Bajo de San Julián itself or in the vicinities of the area where of rhynchonelliform brachiopods as old as the Devonian, the both the Early Miocene Monte León Formation and the San trace is much better documented for Holocene and fossil Julián Formation (Meseta Chica and Gran Bajo Members) are mollusk shells (see Taylor and Wilson 2003 and references exposed. therein). In fact, this type of trace has been commonly found in mollusk shells elsewhere (e.g., Bromley and D’Alessan− dro 1983; Pickerill et al. 1998, 2002; Taylor and Wilson 2003; Lorenzo and Verde 2004; Parras and Casadío 2006). As far as we know, Caulostrepsis has not been documented and/or figured for any shell of Bouchardia species.

Geological setting

Bouchardia rosea shell accumulations.—Brachiopods and mollusks co−occur at many sites along coastal intertidal to the deep subtidal shelf of the Ubatuba Bight, state of SãoPaulo,in the Southeast Brazilian Shelf (Fig. 1). The Ubatuba Bight is characterized by a series of small sedimentary plains delineated by igneous and metamorphic promontories. Continental and transgressive marine Pleistocene and Holocene deposits form these plains (Martin and Suguio 1976; Suguio and Martin 1976; Suguio et al. 1993; Martin et al. 1996; Suguio 1999). The Ubatuba Bight has an average water depth of 10 m and a total area of nearly 8 km2. The bight faces to the east and is therefore protected against the prevailing S−SW trade winds and high− energy waves (Mahiques et al. 1998). However, Ubatuba Bight is influenced by warm waters of the South Brazil Current. The following annual mean values have been reported for the bight waters: temperature: 23.8°C, salinity: 33.2‰, and dissolved 2m oxygen: 5.11 mg/l (Mantellato and Fransozo 1999). Sedimentation rate is considered negligible in the Ubatuba Bight (Magliocca and Kutner 1965; Simões et al. 2004b). 10 m Fine−grained (silt and very fine sand), terrigenous sediments, including an admixture of terrestrial organic matter, character− 0 0 ize the bight bottoms (Mantelatto and Fransozo 1999). Sur− ficial sediments may contain abundant biogenic fragments, including brachiopod Bouchardia rosea (Fig. 3), mollusks, coarse sandstones volcanic rocks echinoids, bryozoans, and foraminifers. However, these are patchily distributed in the area, preferentially occurring in the fine sandstones cross-bedding stratification outer portions of the bight (Mahiques et al. 1998; Mantelatto herringbone cross mudstones and Fransozo 1999; Carroll et al. 2003; Rodland et al. 2004, stratification 2006; Rodrigues 2006). sandy limestones bioturbation Paleogene Bouchardia zitteli shells.—The South Atlantic tuffaceous sandstones Bouchardia beds transgressions in the Eastern sector of the Austral Basin in southern Patagonia (Argentina) across the Paleogene/Neo− Fig. 2. Schematic stratigraphic sections of the studied fossil localities in gene boundary generated several shallow fossil−rich marine Bajo de San Julián, Argentina (A) and Cerro Bautista, Uruguay (B), show− deposits grouped under the informal name of the “Patagonian ing the Bouchardia−beds.

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Following the early work, no future references to Manan− Rios Province), along the Uruguayan coast in the Colonia and tial Salado locality has been made by subsequent researchers San José Departments (Camacho Formation), and in the working in the region. However, some other localities in the southernmost Brazil (Pelotas Basin, the state of Rio Grande do Bajo San Julián−Puerto San Julián’ area where Bouchardia Sul) (Martínez and del Rio 2002). Rocks of Camacho Forma− zitteli has been recorded were reported by del Río (2004) as tion are Late Miocene in age (Figueiras and Broggi 1971; representing the San Julián Formation (upper and lower mem− Herbst and Zabert 1987; Scasso et al. 2001). These include bers). The brachiopods in this unit are associated with the fine to medium sandstones, silty sandstones, fossil−rich lime− echinoids Iheringiella patagonensis and with the Panopea stones, which were deposited in intertidal, foreshore, and sierrana–Parynomya patagonensis bivalve assemblage (del mid−shelf settings. In the Cerro Bautista locality, Uruguay, Río 2004). The San Julián Formation, in its type area in the proximal tempestites are characterized by highly diverse and Bajo San Julián, has been considered of Late Eocene age abundant shelly concentrations (Fig. 2). These are dominated (Camacho 1974), late Eocene–Oligocene (Bertels 1977), by mollusks, brachiopod Bouchardia transplatina (Fig. 3) and while the uppermost horizons have been placed in the Oligo− balanomorphs (Martinez 1994). cene (Barreda 1997) (see del Río 2004 for a discussion of age). Neogene Bouchardia transplatina shells.—During the Neo− gene (Miocene), large areas of the southern region of South Materials and methods America, including Argentina, Uruguay, and Brazil were flooded by the “Entrerriense” transgressions. Fossil−rich de− Bulk samples included a total of 1211 valves of Bouchardia posits are known in Argentina (Puerto Madryn Formation in rosea (Fig. 3) collected from 14 nearshore localities (depth northeastern Patagonia and Paraná Formation in the Entre range: 0–30 m) in the general area of Ubatuba Bight (Fig. 1). For all sampling stations, surficial sediments were collected using a Van Veen grab sampler (1/40 m3) and otter−trawl nets with an anchor dredge. This allowed us to acquire the upper− most several centimeters of bottom sediments, with sample volume totaling at least 8 liters of bottom sediments. The samples were wet−sieved, throughout 8−mm to 2−mm mesh sizes, and air−dried. Brachiopod samples consisted of dead, empty shells and rare specimens collected alive. Following sieving, all living brachiopods (only 10 specimens) were stored in 70% ethanol. To assess the geological record of trace fossils on Bou− chardia shells, the paleontological materials reposited in two scientific collections were examined. In the first collection, housed in IGC−DPE, we identified 80 specimens of Bou− chardia zitteli (Fig. 3) from Manantial Salado locality, San Julián Formation (Oligocene), Argentina. Most (68.7%, n = 55) of these specimens are articulated, and non−fragmented, although they sometimes show evidence (e.g., granular shell texture, pits) for chemical dissolution. In the second collec− tion, housed in FCDP, 135 specimens of B. transplatina (Fig. 3) were studied. These fossils came from Cerro Bautista lo− cality, Camacho Formation (Late Miocene), and are repre− sented by complete, mainly disarticulated (80%, n = 108), and recrystallized shells. Shells of B. rosea, B. zitteli, and B. transplatina were counted and analyzed under the stereomicroscope for the presence of Caulostrepsis Clarke, 1908. Both wall−exposed Fig. 3. General shell morphology of bouchardiid brachiopods. A–C. Bou− traces and tube openings (Fig. 4) were considered as refer− chardia rosea (Mawe, 1823) from modern accumulations from the Ubatuba able to Caulostrepsis. All infested shells were digitally im− coast, State of São Paulo, Brazil. A. Specimen DZP−18669. B. Specimen aged under high magnification, and imported into Corel DZP−18670. C. Specimen DZP−18671. D–F. Bouchardia transplatina Ihe− Draw (version 12) for the trace measurements. Also, selected ring, 1907 from the Cerro Bautista locality, the Camacho Formation, Late specimens were examined under the SEM. The three stan− Miocene, Uruguay. D. Specimen FCDP−2305E. E. Specimen FCDP−2305G. F. Specimen FCDP−2305K. G–I. Bouchardia zitteli Ihering, 1897 from the dard dimensions of brachiopod shells (length, width, and Manantial Salado locality, the San Julian Formation, Late Oligocene, Argen− thickness) were measured with electronic caliper to the near− tina. G. Specimen IGC−DPE−855D. H. Specimen IGC−DPE−865H. I. Speci− est 0.1mm. In the case of Holocene shelly accumulations men IGC−DPE−865N. Scale bars 5 mm. from the Ubatuba Bight, the same procedure was followed RODRIGUES ET AL.—SPIONID—BRACHIOPODS INTERACTION 661 for all bivalve mollusks that co−occurred with Bouchardia rosea. When possible, bivalve specimens were identified to genus level, based on the relevant taxonomic lists (e.g., Abbott and Dance 1982; Ríos 1994). Trace frequencies for both modern and fossil brachio− pods, as well as sympatric bivalve mollusks were computed by dividing number of disarticulated valves by two (see Kowalewski 2002 for a discussion of how to correct fre− quency of single traces for bivalved host organisms). Com− parisons of trace frequencies are presented according to the (i) collecting sites; (ii) shell size; (iii) valve type; (iv) occur− rences on shells of co−occurring groups of organisms (Bou− chardia rosea and bivalve mollusks), and (v) occurrences within Bouchardia, throughout the sampled geological re− cord (Late Oligocene, Late Miocene, and Late Holocene).

Results

Borings in Bouchardia rosea.—Modern (living and empty) shells of Bouchardia rosea typically show boring traces re− Fig. 4. Bioerosion trace Caulostrepsis. A. Specimen DZP−18422, ventral valve of Bouchardia rosea showing the typical morphology of Caulo− ferable to the ichnogenus Caulostrepsis (Fig. 4). Traces are strepsis. Note the well−developed central ridge, and the straight morphol− organized as U−shaped galleries, with the limbs of the U be− ogy of the trace. B, C. Specimens DZP−18423 and 18424, respectively. ing more or less straight longitudinally, quite closely to− Note that the galleries are roughly straight, and not enlarged at their distal gether, and parallel to the plane defined by the inner (or extremities. The apertural groove (arrow) is well marked. D. Specimen outer) surface of the brachiopod shell (euendolithic penetra− DZP−18425, dorsal valve, showing multiple (arrows), straight traces. E, F. tion). In unroofed or roof−less specimens, the sides of the X−ray images of the specimens DZP−18426 and 18427, respectively. Note tube are deeper than the middle, resulting in a typical central the straight morphology of unabraded tubes and the apertural groove (ar− row) in the specimen DZP−18427. Scale bars 5 mm. elongated ridge. Hence, the space between the limbs is open but narrower, so that the cross−sectional tube morphology looks like a broad−centered figure−of−eight morphology. increase in trace frequencies can be observed with increase in Both gallery openings communicate only with the outer sur− the host shell size. For example, when shells were grouped in face of the shells and do not come into contact with the inter− terms of their maximum length (from small to large into three nal soft parts of the host shell. In many cases, the gallery can categories >8 mm, 8–6 mm, and 6–2 mm), trace frequencies extend over the entire length of the brachiopod shell (Fig. 4). were 40.4%, 25.6%, and 19.4%, respectively (Table 2). This Typically, more than one gallery may be present, but never pattern persisted when trace frequencies were analyzed for more than 3 on a single host valve (Fig. 4). Maximum ob− those shell size classes separately for 4 out of 5 collecting served trace length was 17.15 mm, and the maximum width sites (Station UBA5 was the only exception). was 2.0 mm. For all specimens, the width of the tubes tends Pooling the data by valve type, trace frequencies of 28.6% to be approximately constant along their long axis. and 18.0% were observed for dorsal and ventral valves, re− Polychaetes found inside the borings in association with spectively (Table 3). However, the relation is variable across living specimens of Bouchardia rosea are characterized by stations. Dorsal valves showed higher trace frequencies than long and coiled peristomial palps stretching out of the tube. ventral valves in some of the collecting stations (Stations Large chaetae are present on both sides of the 5th segment and a flanged pygidium is also observed (Fig. 5). All speci− Table 1. Number of infested and non−infested, live and dead Bouchardia rosea shells per collecting sites. Trace frequency (TF) estimated by mens of Bouchardia rosea (10 specimens) collected alive sampling sites. Abbreviations: Frag., fragmentation rates; Inf., infested were infested by living polychaetes, as described above. shells; TF, trace frequency. However, none of the 149 dead Bouchardia rosea shells bearing corresponding traces showed any living polychaetes Collecting sites Living specimens Dead shells Depth TF TF Frag. inside the borings. Station Total Inf. Total Inf. Trace frequency in brachiopods was 24.8%, and varied (m) (%) (%) (%) by collecting site, with values ranging substantially across UBA 1 30 0 – – 451 62 27.7 23.7 sampling stations: 10.3% (Station UBA5, 20 m water depth, UBA 4 25 0 – – 113 30 53.1 43.4 Table 1), 20.3% (Station UBA9, 10 m water depth, Table 1), UBA 5 20 0 – – 155 8 10.3 34.2 27.7% (Station UBA1, 30 m water depth, Table 1), and UBA 9 10 10 10 100 482 49 20.3 34.6 53.1% (Station UBA4, 25 m water depth, Table 1). A notable Total 10 10 100 1201 149 24.8 45.6

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Table 2. Number of infested and non−infested dead Bouchardia rosea (Late Oligocene, Argentina), and 135 shells of B. trans− shells per collecting sites and size categories. Abbreviations: Inf., in− platina of Camacho Formation (Late Miocene, Uruguay) fested shells; TF, trace frequency. were also studied (Table 4). For B. zitteli, shell size ranged from 3.3 mm to 19.1 mm (Table 4). Considering the same Collecting Dead shells Dead shells Dead shells sites >8 mm 8–6 mm 6–2 mm standard size classes, as used above for B. rosea shells for this species, 93.7% (n = 75) of the shells are in >8 mm class; Depth TF To− TF TF Station Total Inf. Inf. Total Inf. (m) (%) tal (%) (%) 5% (n = 4) in 8–6 mm class, and 1.3% (n = 1) in 6–2 mm UBA 1 30 3 1 66.6 214 35 32.6 234 26 22.2 class. Among B. transplatina shells, specimens were only grouped in the >8 mm (99.2%, n = 134), and 8–6 mm (0.8%, UBA 4 25 11 3 54.5 25 6 48 77 21 54.6 n = 1) size classes, with shell size ranging from 7.9 mm to UBA 5 20 0 ––500150810.6 20.4 mm (Table 4). For both fossil species, ventral and dorsal UBA 9 10 179 35 39.1 153 10 13 150 4 5.2 valves were well represented in the studied collections. In B. Total 193 39 40.4 397 51 25.6 611 59 19.4 zitteli, 13.7% (n = 11) were ventral valves and 17.6% (n = 14) were dorsal valves, being 68.7% (n = 55) articulated speci− Table 3. Number of infested and non−infested dead Bouchardia rosea mens. In B. transplatina, 36.3% (n = 49) were ventral valves, shells per collecting sites and valve type. Fragmentation rates are also 43.7% (n = 59) were dorsal valves, and 20% (n = 27) were ar− indicated. Abbreviations: Frag., fragmentation rates; Inf., infested ticulated specimens. Both, B. zitteli and B. transplatina are shells; TF, trace frequency. devoid of Caulostrepsis traces (Table 4). Collecting sites Dorsal valves Ventral valves Depth Frag. TF TF Station Total Inf. Total Inf. (m) (%) (%) (%) Discussion UBA 1 30 23.7 368 57 31.0 83 5 12.0 UBA 4 25 43.4 61 17 55.8 52 13 50.0 Bioeroder identity.—U−shaped pouched−like traces (Caulo− UBA 5 20 34.2 39 4 20.6 116 4 6.8 strepsis) are produced by several families of polychaetes UBA 9 10 34.6 300 32 21.4 182 17 18.6 (e.g., Bromley 1994; Parras and Casadío 2006). For exam− Total 768 110 28.6 433 39 18.0 ple, Spionidae (polydorid) polychaetes are known to produce Caulostrepsis (Bromley 1994; Taylor and Wilson 2003). However, Bromley (1978) has suggested that such traces can Table 4. Data for Paleogene and Neogene Bouchardia shells. Abbrevia− be made by Eunicidae polychaetes. Our in vivo observations tions: Art., articulated shell; Frag., fragmentation rate; TF, trace frequency. of polychaetes inside the shells provide direct evidence that Size (mm) Valve type (%) definitive (and not just incipient, see Taylor and Wilson Frag. TF Taxon Total dor− ven− 2003) Caulostrepsis can also be produced by spionid poly− mean min max Art. (%) (%) sal tral chaetes (see also Wisshak and Neumann 2006). The long and B. zitteli 80 13.9 3.3 19.1 68.7 17.5 13.8 16.3 0 coiled peristomial palps, the large chaetae present on both th B. transplatina 135 14.5 7.9 20.4 20.0 43.7 36.3 0.7 0 sides of the 5 segment, and the flanged pygidium (Fig. 5) are all consistent with Polydora sp. (Spionidae). UBA1 and UBA5). On the other hand, comparable trace fre− Among the spionids, 35 species are known to have rela− quencies for dorsal and ventral valves were observed for spec− tionships with diverse invertebrate hosts, including mol− imens collected from Station UBA9 and UBA4 (see Table 3 lusks, sponges, cnidarians, cirripeds, bryozoans, and coral− for details). line algae (Blake and Evans 1973). Data presented here add to the very limited literature doc− Holocene sympatric mollusk bivalve shells.—In total 2086 umenting that rhynchonelliform brachiopods can act as host bivalve valves, from the same collecting stations that yielded for spionids. Until now, Lingula, Terebratalia tranversa, Bouchardia rosea shells, were examined for the occurrence, Terebratulina unguicula, and Laqueus californianus were distribution, and density of Caulostrepsis traces. The bivalve the other known extant brachiopods that may be infested by mollusk specimens were randomly chosen. They represent polychaetes (Hammond 1984; Rodrigues 2007). 36 genera, including 25 infaunal genera (731 shells), 2 semi− Trace morphology.—The trace morphology is similar to infaunal genera (64 shells), 9 epifaunal genera (282 shells), that of Caulostrepsis taeniola and C. cretacea in having a and 1009 unidentifiable shells (Appendix 1). Although drill comparable pouch structure (see Bromley and D’Alessandro holes (Simões et al. 2007a) and encrusting organisms (Rodri− 1983: 297, fig. 7). However, traces found in shells of Bou− gues 2006) are common in those shells, no traces referable to chardia rosea are morphologically much simpler (Fig. 6) Caulostrepsis were identified in the sympatric mollusk bi− than those described by Bromley and D’Alessandro (1983). valve shells of the Ubatuba Bight. Namely, the difference between the Caulostrepsis in Bou− Paleogene and Neogene Bouchardia shells.—A total of 80 chardia rosea shells and C. taeniola (typically found in bi− specimens of Bouchardia zitteli of San Julián Formation valve mollusk shells, among others) is that in the latter the RODRIGUES ET AL.—SPIONID—BRACHIOPODS INTERACTION 663

Fig. 5. Spionid polychaete Polydora sp. found in association with Bouchardia rosea shells, Ubatuba Bight, 10 and 20 m depth. Specimen DZP−18668. A, B. Anterior segments of Polydora showing the characteristic modified chaetae (arrows) in its 5th segment. C. Polydora hooks (arrow) from the median segments. D. Posterior segments of Polydora showing the flanged pygidium (arrow). Scale bars 100 μm. cross sectional shape varied from flat−oval, elliptical or con− stricted to dumbbell (see Bromley and D’Alessandro 1983: 297, fig. 7), and in the former only a figure−of−eight morphol− ogy was present along the whole trace (Fig. 6). However, in some cases, the central ridge resulted from the fusion of the limbs was not preserved throughout the trace. The ecological interaction of the Caulostrepsis in Bou− chardia rosea: the time of infestation.—As commented above, none of the Caulostrepsis found in dead shells was in− habited by a polychaete (also, spionid soft tissues from a dead infester was not recovered from any of the dead shells). In addition, in all studied shells the tubes were located on the external side of the host valve, never inside the valve, and the 5mm tubes always opened to the outside of the shell. These obser− vations suggest consistently that infestation events occurred preferentially when the host was still alive. As observed by Fig. 6. Morphology of Caulostrepsis. A, B. Drawings of Caulostrepsis Pickerill (1976), infestation of living host seems advanta− taeniola Clarke, 1908 (A) and Caulostrepsis cretacea (Voigt, 1971) (B), re− geous to some infestors, because such hosts provide better spectively. C. Morphology of Caulostrepsis traces found in Bouchardia protection from overturning, breakage or abrasion relative to rosea shells. Note differences in the cross−sectional morphology between empty valves or shells. the traces reported here (C) and those documented previously (A, B).

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The syn−vivo infestation postulated here is consistent with mulations include relatively few ventral valves comparing similar data collected recently for the brachiopod fauna of San with dorsal ones (i.e., estimates of infestation frequencies are Juan Island (USA), Pacific Ocean (Rodrigues 2007). As for B. prone to have very large error due to a relatively smaller sam− rosea, living shells of Terebratalia tranversa, Terebratulina ple size of ventral valves). In general, brachiopod valve accu− unguicula,andLaqueus californianus appear to be colonized mulations from most sites (Table 3) appear to have been af− by polychaetes only when they are alive. Similarly, none of fected by a bias favoring preservation of dorsal valves. This polychaete traces opened inward, and the presence of blisters bias is, most likely, due to taphonomic processes such as hy− in shells of Terebratalia tranversa, Terebratulina unguicula, drodynamic sorting and differential shell dissolution (Simões and Laqueus californianus suggests strongly that the penetra− et al. 2007b). Indeed, in the case of a sample with equal pro− tion occurred when those brachiopods were still alive (Rodri− portion of ventral and dorsal shells (Station UBA4, Table 3), gues 2007). In the case of B. rosea shells, no blisters associ− the trace frequencies per valve type is similar (TFdorsal = ated with Caulostrepsis were observed. However, it should be 55.8%; TFventral = 50%, Table 3). noted that the absence of blisters in this species is probably due As recently demonstrated by Rodrigues (2007), the bra− to the thick−shelled nature (the secondary fibrous layer is very chiopod mode of live may play an important role in the stereo− thick) of Bouchardia rosea shell; the Pacific shells are rela− typy of the trace producers. For example, shells of Terebratalia tively much thinner. Our data are also consistent with multiple tranversa, Terebratulina unguicula,andLaqueus californi− studies focused on other types of host. For example, Parras anus collected from rocky and muddy substrates, from Pacific and Casadío (2006) demonstrated that polychaete borings Ocean, around San Juan Islands (USA), exhibited traces pref− (e.g., Maeandropolydora) in Paleocene and Neogene oysters erentially distributed on ventral valves, even considering living were made while they were alive. Wisshak and Neumann specimens only (Rodrigues 2007). These brachiopods are epi− (2006) suggested that Caulostrepis traces in the Cretaceous faunal, sessile, attached to the substrate, lying on dorsal valve. (Early Maastrichtian) echinoid Echinocorys ovata are evi− Thus, ventral valves of living specimens offer the most advan− dence of syn−vivo infestation of the oral surface of host shell tageous location (maximally elevated above the sediment−wa− by polydorid polychaetes. Finally, living specimens of bivalve ter interface) for the settlement of a suspension−feeding infester mollusks (Chione fluctifraga) from Bahía Falsa, Baja Califor− (Rodrigues 2007). This mode of life contrasts with the free−liv− nia, and Bahía de Guásimas, Sonora, were kept in aquaria and ing mode of B. rosea. Shells of this species are not firmly at− also showed infestation by Polydora (Caceres−Martinez et al. tached to the substrate (see Brunton 1996; Richardson 1981, 1999). These laboratory studies demonstrated that shell tubes 1987; Simões et al. 2004a, 2007a) and are prone to lateral were occupied by living polychaetes, most of the time located transport and reworking. Hence, the similar rates of infestation around the siphon area of the host shell. Although polychaetes for dorsal/ventral valves of Bouchardia rosea may reflect the were able to survive in recently dead shells, new infestations free−living mode of life of this brachiopod. of dead hosts were not observed (Caceres−Martinez et al. 1999). In all 10 specimens of B. rosea collected alive, infesting polychaetes (Polydora sp.) were found in direct physical as− The nature of the ecological interaction between Caulo− sociation with brachiopod shells, living inside Caulostrepsis. strepsis and Bouchardia rosea.—The high infestation rates These traces were not observed in the sympatric mollusk bi− (24.8%, pooled data) observed for Bouchardia rosea shells is valves. Hence, this interaction is not a result of a fortuitous consistent with the fact that spionid polychaetes are wide− encounter of polychaete larvae and the host brachiopod shell. spread and abundant in the study area (Paiva 1996; Petti 1997; The seafloors in the study area are devoid of large clasts and Santos 1998; de Léo 2003; Amaral and Nallin 2004). In spite bioclasts. In many cases, dense accumulations of B. rosea of the fact that brachiopod shells were bored by polychaetes shells (Simões et al. 2007b) are the main hard substrate avail− when they were alive, it is difficult to determine if this ecologi− able. Notably, the dense accumulations are near the islands cal interaction represents commensal or parasitic relationship. and/or in other places (Station UBA9) characterized by lo− In part, this is because studies dealing with the metabolic costs cally high rates of primary productivity. inflicted on brachiopods by infesting spionids are lacking. Ad− Given the notable−to−high frequencies of spionid−infested ditionally, all inferred cases of commensalism/parasitism in− shells observed across Recent sites for B. rosea, the complete volving rhynchonelliform brachiopods were based on indirect lack of evidence for such interactions in fossil specimens of B. inferences. Nevertheless, some observations regarding the na− zitteli and B. transplatina is intriguing. Especially when con− ture of the biotic interaction can be made. sidering that these fossil occurrences represent similar climatic A commensal rather than parasitic interaction seems to be and environmental settings and the producers of Caulostrepsis more likely in the case of the Polydora–Bouchardia rosea in− are known to have been present in the Cenozoic ecosystems of teraction because of the mode of life of the hosting shell and the southern South America. Samples of the oyster the lack of valve and surface site stereotypy. As indicated by Crassostrea? hatcheri from Paleogene deposits of Argentina the data in Table 3, there is no preference (stereotypy) for the (the San Julián Formation, Late Oligocene), show very high type of valve colonized by the borers. The high rates of trace frequencies (97%) of Caulostrepsis and Maeandropolydora observed on dorsal valves from Station UBA1 and Station traces (Parras and Casadio 2006). Comparably high frequen− UBA5 may be a taphonomic artifact, since these shell accu− cies were reported for oysters recovered from the Centinela RODRIGUES ET AL.—SPIONID—BRACHIOPODS INTERACTION 665

Formation (Early Miocene) from Argentina (Parras and Ubatuba Bight, some shell fragments of B. rosea are clearly Casadio 2006). Additionally, Caulostrepsis is a common trace the result of breakage along the surface defined by polychaete in mollusk shells of Neogene rocks from the Uruguay tubes (Caulostrepsis), especially when the trace was located (Lorenzo and Verde 2004), including bivalve shells of the near the maximally convex part of the shell (Fig. 7). Camacho Formation (Late Miocene, Mariano Verde personal communication 2005), a unit known to contain Bouchardia− dominated shell beds. Given the absence of infested shells in fossil brachiopods, at least on shells of those considered scientific collections, and the absence of infested bivalve shells co−occurring with in− fested bouchardiid shells in the Holocene, it is possible that the spionid−brachiopod interaction may represent an evolutio− narily recent development. In addition, observations on the Eocene Bouchardia antarctica shells can support this inter− pretation, due to the lack of any trace of spionid−brachiopod interaction on over 300 specimens (Bitner 1996; Maria A. Bitner, personal communication 2008). However, given the 5mm limited scope of our fossil data, both in terms of the number of fossil specimens examined and the number of fossil sites sam− Fig. 7. Fragments of Bouchardia rosea (Mawe, 1823) shells resulting from pled, the absence of polychaete traces may reflect inadequate the breakage along the surface defined by polychaete tubes. sampling. Further studies are required, especially in the youn− ger part of the Neogene to evaluate the putative hypothesis that It is noteworthy that the highest frequency of infested the spionid−brachiopod interaction is geologically recent. shells observed at Station UBA4 (53.1%) is more likely to be a Regardless of its geological history, frequent spionid infes− consequence of higher level of taphonomic alteration at this tations of B. rosea cannot be viewed as a geographically local, site than a reflection of elevated rates of biological infestation. spatially unique phenomenon restricted to the Ubatuba Bight: That is, spionid traces tend to be much more difficult to detect Bouchardia rosea shells found in the Santos Bight (~100 kilo− in unaltered Bouchardia rosea shells (see X−ray of fresh meters south of the study area) and at the Maricá Beach, Rio shells; Fig. 4) because infestation of pristine shells is only de Janeiro coast (~187 kilometers northward of the study area) manifested by their small tube openings. In contrast, heavily also often bear Caulostrepsis traces (Rodrigues and Simões abraded/corroded shells and shell fragments broken along the 2007, SCR personal observation). trace facilitate identification by making Caulostrepsis well− Finally, the spionid−brachiopod interaction here described exposed and often marked by its distinct central ridge structure may represent a very specific biotic relationship, since Caulo− (Fig. 4). In this context, it is noteworthy that Station UBA4, strepsis traces are not recorded on shells of other co−occurring where Bouchardia shell fragments are very common (43.4%; benthos. Table 3), is also the site that yielded the highest frequencies of Taphonomic implications of Caulostrepsis in brachiopod polychaete borings (53.1%; Table 1). Thus, the infested B. shells.—In their exhaustive review of the fragmentation of rosea shells offer an example of an interesting taphonomic bioclastic materials, Zuschin et al. (2003) showed that multi− feedback, where traces induce biological facilitated fragmen− ple factors are responsible for shell fragmentation in different tation, but that fragmentation occurs along the trace facilitat− sedimentary settings. For example, fragmentation may be due ing detection and identification of the ecological information to ecological interactions, as a result of feeding activities represented by Caulostrepsis (Fig. 7). Such fragments, if pre− among members of a given community (Zuschin et al. 2003). served, should offer a rich source of paleoecological and Drilling, chipping, crushing, peeling, rasping, breaking, and ichnological data in the fossil record. The fossilized fragments microbioerosion of hard parts are some of the damages pro− of B. zitteli and B. transplatina valves yielded no Caulo− duced on shelly organisms by gastropods, calappid crabs, strepsis, reinforcing the notion that those fossils came from spiny lobsters, fishes, birds (oystercatchers), cyanobacteria, populations that had not been infested by spionids. algae, fungi, and many other biological agents. These interac− Finally, it should be noted that multiple fossil examples tions may weaken shells making the resulting bioclasts more documenting interactions between brachiopods and some prone to fragmentation (Zuschin et al. 2003: 59). However, ancient infesters were provided previously for several Paleo− fragmentation induced by ecological processes is difficult to zoic brachiopod taxa (e.g., Clarke 1908; Chatterton 1975; recognize in death and fossil assemblages, because resistance Rodriguez and Gutschick 1977; Vinn 2005; Daley 2008), to lethal damage by durophagous predators often cannot be di− The syn−vivo interactions between Polydora sp. and B. rosea rectly assessed (see Zuschin et al. 2003, for a review). How− documented here offer a useful modern analog that can aug− ever, in the case of B. rosea shells, patterns of shell breakage ment ecological, behavioral, and taphonomic interpretations may be linked to a specific causative agent. Namely, in the of infestation in ancient brachiopods.

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Amaral, A.C.Z. and Nallin, S.A.H. 2004. Catálogo das espécies dos Annelida Conclusions Polychaeta da costa brasileira. 106 pp. Campinas, SãoPaulo. Barreda, V. 1997. Palinoestratigrafia de la Formación San Julián en el área · This report provides direct present−day evidence for syn− de Playa La Mina (provincia de Santa Cruz), Oligoceno de la Cuenca vivo biotic interactions between spionid polychaetes Austral. Ameghiniana 34: 283–294. (Spionidae, Polydora sp.) and their rhynchonelliform Barrier, P. and d’Alessandro, A. 1985. Structures biogeniques et physiques brachiopod hosts (see also Rodrigues 2007); dans les sables de Pavigliana Reggio Calabria (Italie). Rivista Italiana di · Paleontologia e Stratigrafia 91: 379–408. Spionids responsible for Caulostrepsis traces were ob− Bertels, A. 1970. Sobre el “Piso Patagoniano” y la representación de la served only in life−collected brachiopods providing thus a Epoca del Oligoceno en la Patagonia austral, República Argentina. compelling example for Caulostrepsis traces that are pre− Revista de la Asociación Geológica Argentina 25: 495–501. dominantly (or perhaps even exclusively) pre−mortem Bertels, A. 1977. Estratigrafía y micropaleontología de la Formación San rather than post−mortem in nature. Consequently, the use Julián en su área tipo, Provincia de Santa Cruz, República Argentina. of such bioerosion traces as an indicator of a prolonged Ameghiniana 14: 233–293. Bitner, M.A. 1996. Encrusters and borers of brachiopods from the La Meseta post−mortem exposure to taphonomic processes may not Formation (Eocene) of Seymour Island. Polish Polar Research 17: 21–28. be warranted unless unambiguous evidence exists to vali− Blake, J.A. and Evans, J.W. 1973. Polydora and related genera as borers in date such traces as post−mortem (e.g., location in shell re− mollusk shells and others calcareous substrates. Veliger 15: 235–249. gions that could not have been inhabited if the brachiopod Bromley, R.G. 1978. Bioerosion of Bermuda reefs. Palaeogeography, host had been alive at the time of infestation); Palaeoclimatology, Palaeoecology 23: 169–197. · Even though Caulostrepsis traces occur syn−vivo, they do Bromley, R.G. 1994. The palaeoecology of bioerosion, In: S.K. Donovan (ed.), The Palaeobiology of Trace Fossils, 134–154. John Wiley and nevertheless weaken shells and make them more prone to Sons, Chichester. fragmentation. Fortuitously, the fragmentation often oc− Bromley, R.G. and D’Alessandro, A. 1983. Bioerosion in the Pleistocene curs via breakage along the surfaces defined by the traces. of southern Italy: ichnogenera Caulostrepsis and Maeandropolydora. Thus, this biological facilitated fragmentation can be eas− Rivista Italiana di Paleontologia e Stratigrafia 89: 283–309. ily recognized in death assemblages and makes polychaete Brunton, C.H.C. 1996. The functional morphology of the Recent brachio− Bouchardia rosea Acta Zoologica traces more noticeable; pod . 77: 233–240. · Cáceres−Martinez, J., Tinoco, G.D., Bustamante, M.L.U., and Gómez− The complete absence of spionid borings in Holocene Humaran, I.M. 1999. Relationship between the burrowing polychaetes sympatric bivalve shells and the fact that Bouchardia fos− Polydora sp. and the black clam Chione fluctifraga Sowerby. Journal of sils were not infested by such traces despite the fact that Shellfish Reasearch 18: 85–89. Caulostrepsis traces were common in fossil bivalve shells, Camacho, H.H. 1974. Bioestratigrafía de las formaciones marinas del both suggest that the Spionidae−Bouchardia association Eoceno y Oligoceno de la Patagonia. Anales de la Academia Nacional de Ciencias Exactas, Físicas y Naturales de Buenos Aires 26: 39–57. may be geologically young, and possible very specific, bi− Carroll, M., Kowalewski, M., Simões, M.G., and Goodfriend, G.A. 2003. ologic interaction. However, the absence of traces in fossil Quantitative estimates of time−averaging in brachiopod shell accumula− brachiopods may also reflect limited number of fossil sites tions from a modern tropical shelf. Paleobiology 29: 382–403. and fossil brachiopod specimens that were accessible for Chatterton, B.D.E. 1975. A commensal relationship between a small filter this project. feeding organism and Australian Devonian spiriferid brachiopods. Paleobiology 1: 371–378. Clarke, J.M. 1908. The beginnings of dependent life. New York State Mu− seum Bulletin 121: 149–169. Acknowledgments Daley, A.C. 2008. Statistical analysis of mixed−motive shell borings in Or− dovician, Silurian, and Devonian brachiopods from northern and east− Funding for this project was provided by the São Paulo State Science ern Canada. Canadian Journal of Earth Sciences 45: 213–229. Foundation (FAPESP), grants 00/12659−7 and 02/13552−7, and CNPq de Léo, F. 2003. Estrutura e dinâmica da fauna bêntica em regiões da plata− (the Federal Agency of Sciences, Brazil). The study was also supported forma e talude superior do Atlântico Sudoeste. 163 pp. Unpublished M.Sc. by the National Science Foundation (OCE−0602375) and Petroleum thesis. Instituto Oceanográfico, Universidade de SãoPaulo. Research Fund AC−PRF (40735−AC2) grants to MK. Personal thanks del Río, C.J. 2004. Tertiary marine Molluscan Assemblages of Eastern are extended to Adilson Fransozo (DZP) for providing assistance dur− Patagonia (Argentina): a biostratigraphic analysis. Journal of Paleon− ing the sampling program in the study area. Luiz Eduardo Anelli tology 78: 1097–1122. (Departamento de Geologia Sedimentar e Ambiental, USP, Sao Paulo, Figueiras, A. and Broggi, J. 1971. Estado actual de nuestros conocimientos Brazil) kindly offered fossil bouchardiid specimens used in this study. sobre los moluscos fósiles del Uruguay. III (cont.). Comunicaciones de We also thank Maria A. Bitner (Institute of Paleobiology PAS, War− la Sociedad Malacológica del Uruguay 3 (21): 131–154. saw, Poland), Christan C. Emig (Centre d’Océanologie, Marseille, Hammond, L.S. 1984. Epibiota from the valves of Recent Lingula (Brachio− France), Pat Hutchings (Australian Museum, Sydney, Australia), and poda). Journal of Paleontology 58: 1527–1531. Max Wisshak (Institute of Palaeontology, Erlangen, Germany) for de− Herbst, R. and Zabert, L.L. 1987. Microfauna de la Fm. Paraná (Mioceno Su− tailed reviews that greatly improved this manuscript. perior) de la Cuenca Chaco−Paranense (Argentina). Facena 7: 165–206. Ihering, H. von 1907. Les mollusques fossils du Tertaire et du Crétacé supérieur de l’Argentina. Annales del Museo Nacional de Buenos Aires Series 3A 7: 469–481. References Kowalewski, M. 2002. The fossil record of predation: An overview of ana− lytical methods: In: M. Kowalewski and P.H. Kelley (eds.), The Fossil Abbott, R.T. and Dance, A. 1982. Compendium of Seashells. 280 pp. E.P. Record of Predation: Paleontological Society Special Papers 8: 3–42. Dutton Inc., New York. Kowalewski, M., Simões, M.G., Carroll, M., and Rodland, D.L. 2002. RODRIGUES ET AL.—SPIONID—BRACHIOPODS INTERACTION 667

Abundant brachiopods on a tropical, upwelling−influences shelf (south− Rodland, D.L., Kowalewski, M., Simões, M.G., and Carroll, M. 2004. Colo− east Brazilian Bight, South Atlantic). Palaios 17: 277–286. nization of a “Lost World”: encrustation patterns in modern subtropical Lorenzo, N. and Verde, M. 2004. Estructuras de bioerosión en moluscos brachiopod assemblages. Palaios 19: 384–399. marinos de la Formación Villa Soriano (Pleistoceno Tardío–Holoceno) Rodland, D.L., Kowalewski, M., Carroll, M., and Simões, M.G. 2006. The de Uruguay. Revista Brasileira de Paleontologia 7: 319–328. temporal resolution of epibiont assemblages: are they ecological snap− MacKinnon, D.I. and Lee, D.E. 2006. Bouchardioidea. In: R.L. Kaesler shots or overexposures? Journal of Geology 114: 313–324. (ed.) Treatise of Invertebrate Paleontology, Part H, Brachiopoda, Re− Rodrigues, M., Mahiques, M.M. de, and Tessler, M.G. 2002. Sedimentação vised, Volume 5, 2223–2225. Geological Society of America, Boulder, atual nas enseadas de Ubatumirim e Picinguaba, região norte de Ubatuba, and University of Kansas Press, Lawrence. Estado de São Paulo, Brasil. Revista Brasileira de Oceanografia 50: Magliocca, A. and Kurtner, A.S. 1965. Sedimentos de fundo da Enseada do 27–45. Flamengo, Ubatuba. Contribuições do Instituto Oceanográfico 198: Rodrigues, S.C. 2006. Tafonomia de moluscos bivalves e braquiópodes das 1–15. enseadas de Ubatuba e Picinguaba, norte do Estado de São Paulo: Mahiques, M.M. de, Tessler, M.G., and Furtado, V.V. 1998. Characteriza− implicações do uso de assinaturas tafonômicas no reconhecimento de tion of energy gradient in enclosed bays of Ubatuba region, Southeast− gradientes ambientais. 118 pp. Unpublished Ph.D. thesis, Instituto de ern Brazil. Estuarine, Coastal and Shelf Science 47: 431–446. Geociências, Universidade de São Paulo. Mahiques, M.M. de, Tessler, M.G., Ciotti, A.M., Silveira, I.C.A., Sousa, Rodrigues, S.C. 2007. Biotic interactions recorded in shells of recent S.H.M., Figueira, R.C.L., Tassinari, C.C.G., Furtado, V.V., and Passos, Rhynchonelliform brachiopods from San Juan Island, USA. Journal of R.F. 2004. Hydrodynamically−driven patterns of recent sedimentation Shellfish Research 26: 241–252. in the shelf and upper slope off southeast Brazil. Continental Shelf Re− Rodriguez, J. and Gutschick, R.C. 1977. Barnacle borings in live and dead search 24: 1685–1697. hosts from the Louisiana Limestone (Fammenian) of Missouri. Journal Manceñido, M.C. and Griffin, M. 1988. Distribution and environmental sig− of Paleontology 51: 718–724. nificance of the genus Bouchardia (Brachiopoda, Terebratellidina): Its Santos, M.F.L. 1998. Estrutura e dinâmica da macrofauna bêntica da enseada bearing on the Cenozoic evolution of the South Atlantic. Revista de Ubatuba, litoral norte de São Paulo, Brasil. 155 pp. Unpublished Ph.D. Brasileira de Geociências 18: 201–211. thesis, Instituto Oceanográfico, Universidade de SãoPaulo. Mantelatto, F.L.M. and Fransozo, A. 1999. Characterization of the physical Scasso R.A., McArthur J.M., del Río, C.J., Martínez, S., and Thirlwall M.F. and chemical parameters of Ubatuba Bay, northern coast of São Paulo 2001. 87Sr/86Sr Late Miocene age of fossil molluscs in the “Entrerriense” State, Brazil. Revista Brasileira de Biologia 59: 23–31. of the Valdés Península (Chubut, Argentina). Journal of South American Martin, L. and Suguio, K. 1976. O quaternário marinho do litoral do Estado Earth Sciences 14: 319–327. Anais de São Paulo. XXIX Congresso Brasileiro de Geologia. 1: Simões, M.G., Kowalewski, M., Mello, L.H.C., Rodland, D.L., and Carroll, 281–293. M. 2004a. Present−day terebratulid brachiopods from the southern Bra− Martin, L., Suguio, K., Flexor, J.M., Dominguez, J.M.L., and Bittiencourt, zilian Shelf: Paleontological and biogeographic implications. Palaeon− C.S.P. 1996. Quaternary sea−level history and variation in dynamics tology 47: 515–532. along the central Brazilian coast: consequences on coastal plain con− Simões, M.G., Kowalewski, M., Carroll, M., Barbour−Wood, S., Krause, struction. Anais da Academia Brasileira de Ciências 68: 303–354. R.A.J., Rodrigues, S.C., and Wehmiller, J.F. 2004b. Taphonomy and Martínez, S. 1994. Bioestratigrafía (Invertebrados) de la Formación Cama− time averaging as a tool in (paleo)oceanography: a case study on a shal− cho (Mioceno, Uruguay). Unpublished Ph.D. thesis, 346 pp. Univer− low subtropical shelf from Brazil. In: XLII Congresso Brasileiro de sidad de Buenos Aires, Argentina. Geologia. Anais S−27: 696. Martínez, S. and del Río, C.J. 2002. Late Miocene Molluscs From the South− Simões, M.G., Rodrigues, S.C., and Kowalewski, M. 2007a. Comparative western Atlantic Ocean (Argentina and Uruguay): A Palaeobiogeo− analysis of drilling frequencies in Recent brachiopod−mollusk associa− graphic Analysis. Palaeogeography, Palaeoclimatology, Palaeoecol− tions from the Southern Brazilian Shelf. Palaios 22: 141–152. ogy 188: 167–187. Paiva, P.C. 1996. Variação espacial e temporal da macrofauna bentônica Simões, M.G., Rodrigues, S.C., Leme, J.M., and Pires−Domingues, R.A., da enseada de Picinguaba, Ubatuba, SP: relevância no planejamento 2007b. Brachiopod shells on the beach: taphonomic Overprinting in a amostral em estudos oceanográficos e de monitoramento ambiental de fair−weather shell accumulation and their paleoecological implications. Journal of Taphonomy fundos marinhos inconsolidados. Unpublished Ph.D. thesis. 102 pp. 5 (4): 205–225. Instituto Oceanográfico, Universidade de São Paulo. Suguio, K. 1999. Geologia do Quaternário e mudanças ambientais: passa− Parras, A. and Casadío, S. 2006. The Oyster Crassostrea? hatcheri (Ortmann, do + presente = futuro? 366 pp. Paulo’s Editora, São Paulo. 1897), a Physical Ecosystem Engineer from the Upper Oligocene–Lower Suguio, K. and Martin, L. 1976. Mecanismo de gênese das planícies sedi− Miocene of Patagonia, Southern Argentina. Palaios 21: 168–186. mentares quaternárias do litoral do Estado de São Paulo do Estado de Petti, M.A.V. 1997. Macrofauna bentônica de fundos inconsolidados das São Paulo. In: XXIX Congresso Brasileiro de Geologia. Anais 1: 295. enseadas de Picinguaba e Ubatumirim e plataforma interna adjacente, Suguio, K., Absy, M.L., Flexor, J.M., Ledru, M.P., Martin, L., Sifeddine Ubatuba, São Paulo. 163 pp. Unpublished Ph.D. thesis, Instituto Oceano− Soubiès, F., Turcq, B., and Ybert, J.P. 1993. The evolution of the conti− gráfico, Universidade de SãoPaulo. nental and coastal environments during the last climatic cycle in Brazil Pickerill, R.K. 1976. Vermiforichnus borings from the Ordovician of Cen− (120 KY. B.P. to Present). Boletim IG−USP Série Científica 24: 27–41. tral Wales. Geological Magazine 113: 159–164. Taylor, P.D. and Wilson, M.A. 2003. Palaeoecology and evolution of ma− Pickerill, R.K., Donovan, S.K., and Portell, R.W. 1998. Ichnology of the rine hard substrate communities. Earth−Science Reviews 62: 1–103. Late Pleistocene Port Morant Formation of Southeastern Jamaica. Ca− Tommasi, L.R. 1970. Sobre o braquiópode Bouchardia rosea (Mawe, 1823). ribbean Journal of Science 34: 12–32. Boletim do Instituto Oceanográfico 19: 33–42. Pickerill, R.K., Donovan, S.K., and Portell, R.W. 2002. Bioerosional trace Vinn, O. 2005. The distribution of polychaetes borings in brachiopod shells fossils from the Miocene of Carriacou, Lesser Antilles. Caribbean from the Caradoc Oil Shale of Estonia. Notebooks on Geology 3: 1–11. Journal of Science 38: 106–117. Wisshak, M. and Neumann, C. 2006. A symbiotic association of a boring Richardson, J.R. 1981. Brachiopods and pedicles. Paleobiology 7: 87–95. polychaete and an echinoid from the Late Cretaceous of Germany. Acta Richardson, J.R. 1987. Brachiopods from carbonate sands of the Australian Palaeontologica Polonica 51: 589–597. shelf. Proceedings of the Royal Society of Victoria 99: 37–50. Zuschin, M., Stachowitsch, M., and Staton, R.J. Jr. 2003. Patterns and pro− Ríos, E. de C. 1994. Seashells of Brazil. Segunda edição. 368 pp. Editora cesses of shell fragmentation in modern and ancient marine environ− Fundação Universidade do Rio Grande, Rio Grande. ments. Earth−Science Reviews 63: 33–82.

http://app.pan.pl/acta53/app53−657.pdf 668 ACTA PALAEONTOLOGICA POLONICA 53 (4), 2008 Appendix 1

Number of modern bivalve mollusk shells from collecting stations that also yielded Bouchardia rosea specimens.

Bivalve mollusk Collecting sites Shells Taxa Mode of life UBA 1 (30 m) UBA 4 (25 m) UBA 5 (20 m) UBA 9 (10 m) Total Infested Anomia epifaunal 0 0 1 2 3 0 Arca epifaunal 0 0 0 15 15 0 Chlamys epifaunal 6 3 3 6 18 0 Crassinella epifaunal 0 0 1 2 3 0 Mytilus epifaunal 0 0 0 13 13 0 Ostrea epifaunal 9 18 24 56 107 0 Pecten epifaunal 7 7 11 7 32 0 Pinna epifaunal 7 0 3 0 10 0 Plicatula epifaunal 59 7 16 9 91 0 Anadara semi−infaunal 1 21 10 19 51 0 Atrina semi−infaunal 0 1 1 0 2 0 Adrana infaunal 2 8 11 0 21 0 Amiantes infaunal 4 3 5 2 14 0 Anomalocardia infaunal 0 64 11 0 75 0 Cardita infaunal 0 0 0 1 1 0 Cardium infaunal 0 0 1 0 1 0 Chione infaunal 8 11 8 18 45 0 Corbula infaunal 2 4 10 26 42 0 Diplodonta infaunal 0 2 2 0 4 0 Divaricella infaunal 0 0 3 0 3 0 Donax infaunal 1 0 5 0 6 0 Dosinia infaunal 0 0 2 3 5 0 Glycymeris infaunal 6 2 11 10 29 0 Lucina infaunal 3 3 1 3 10 0 Mactra infaunal 24 29 138 8 199 0 Mya infaunal 0 0 0 3 3 0 Nemocardium infaunal 0 2 0 0 2 0 Nucula infaunal 0 4 5 0 9 0 Periploma infaunal 2 1 0 0 3 0 Pitar infaunal 0 1 0 10 11 0 Raeta infaunal 0 2 2 0 4 0 Semele infaunal 31 18 40 8 97 0 Solen infaunal 1 0 2 17 20 0 Spisula infaunal 0 4 7 4 15 0 Tagelus infaunal 0 2 0 1 3 0 Tellina infaunal 10 10 35 12 67 0 Trachycardium infaunal 0 0 1 40 41 0 Undetermined undetermined 335 222 213 240 1010 0